CT Angiography in the Diagnosis of Brain Death - Semantic Scholar

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Nov 15, 2014 - 1 Department of Diagnostic Imaging and Interventional Radiology, Pomeranian Medical University in Szczecin, Szczecin,. Poland. 2 Clinic of ...
Signature: © Pol J Radiol, 2014; 79: 417-421 DOI: 10.12659/PJR.891114

Received: 2014.05.30 Accepted: 2014.06.09 Published: 2014.11.15 Authors’ Contribution: A Study Design B Data Collection C Statistical Analysis D Data Interpretation E Manuscript Preparation F Literature Search G Funds Collection

REVIEW ARTICLE

CT Angiography in the Diagnosis of Brain Death Marcin Sawicki1 ABCDEF, Romuald Bohatyrewicz2 ADF, Anna Walecka1 DF, Joanna Sołek-Pastuszka2 B, Olgierd Rowiński3 A, Jerzy Walecki4 AD 1 Department of Diagnostic Imaging and Interventional Radiology, Pomeranian Medical University in Szczecin, Szczecin,

Poland

2 Clinic of Anesthesiology and Intensive Care, Pomeranian Medical University in Szczecin, Szczecin, Poland 3 2nd Department of Clinical Radiology, Medical University of Warsaw, Warsaw, Poland 4 Centre of Postgraduate Medical Education, Warsaw, Poland

Author’s address: Marcin Sawicki, Department of Diagnostic Imaging and Interventional Radiology, Pomeranian Medical University in Szczecin, Szczecin, Poland, e-mail: [email protected]

Summary

Brain death is defined as the irreversible cessation of functioning of the entire brain, including the brainstem. Brain death is principally established using clinical criteria including coma, absence of brainstem reflexes and loss of central drive to breathe assessed with apnea test. In situations in which clinical testing cannot be performed or when uncertainty exists about the reliability of its parts due to confounding conditions ancillary tests (i.a. imaging studies) may be useful. The objective of ancillary tests in the diagnosis of brain death is to demonstrate the absence of cerebral electrical activity (EEG and evoked potentials) or cerebral circulatory arrest. In clinical practice catheter cerebral angiography, perfusion scintigraphy, transcranial Doppler sonography, CT angiography and MR angiography are used. Other methods, like perfusion CT, xenon CT, MR spectroscopy, diffusion weighted MRI and functional MRI are being studied as potentially useful in the diagnosis of brain death. CT angiography has recently attracted attention as a promising alternative to catheter angiography – a reference test in the diagnosis of brain death. Since 1998 several major studies were published and national guidelines were introduced in several countries (e.g. in France, Austria, Switzerland, the Netherlands and Canada). This paper reviews technique, characteristic findings and criteria for the diagnosis of cerebral circulatory arrest in CT angiography.



Brain Death • Cerebral Angiography • Multidetector Computed Tomography

MeSH eywords:



PDF fi­le: http://www.polradiol.com/abstract/index/idArt/891114

Background The diagnosis of brain death (BD) is of particular importance in view of the contemporary medical and technological achievements in supporting, repairing and replacing failing human organs. The declaration of BD determines the termination of futile life support and potential procurement of organs for transplantation. Brain death is defined as the irreversible cessation of functioning of the entire brain, including the brainstem with two pathways to reach that point: (i) permanent absence of circulation or (ii) subsequent to a catastrophic brain injury [1]. To determine BD physicians must: • determine the presence of unresponsive coma, • determine the absence of brainstem reflexes,

• determine the absence of respiratory drive after a CO2 challenge – apnea testing. To ensure that the cessation of brain function is “irreversible” physicians must: • determine the cause of coma, • exclude mimicking medical conditions, • observe the patient for a period of time to exclude the possibility of recovery [2]. Confounding conditions that may invalidate testing for cessation of brain function include: hypothermia; the use of therapeutic hypothermia; the presence of central nervous system depressing drugs that may explain or contribute to coma; high cervical spine injury; acquired or therapeutic neuromuscular paralysis; and severe acid-base, electrolyte,

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Figure 1. The case of a 22-year-old woman with brain stem ischemic stroke and right-sided craniectomy presenting signs of BD on clinical examination; (A) – 10-mm MIP in the sagittal plane in CTA shows opacification of the right pericallosal artery (thin arrows); (B) – 10-mm MIP in the coronal plane in CTA shows opacification of M1 segments of MCAs (thin arrows). endocrine abnormality that may explain or contribute to coma [3].

Normal CBF at rest is maintained within a range of 45–60 mL/100 g of brain tissue/min. A brain injury is accompanied by cerebral edema. Because the skull bones When uncertainty exists about the reliability of parts of limit the intracranial volume this “mass effect” leads to the clinical examination or when the apnea test cannot be the intracranial hypertension. The process spreads from performed ancillary tests may be useful. The objective of the region of primary injury gradually involving the whole ancillary tests is to demonstrate the absence of cerebral brain and the intracranial vessels become compressed but electrical activity (EEG and evoked potentials) or cerebral preserve their patency. Initially CVR is kept almost concirculatory arrest. A number of blood flow tests were introstant by the activated autoregulation mechanisms releasing of ancillary testsduced is to demonstrate the absence of cerebralcatheter electricalcerebral activity (EEGblood and vessel tone. However, this phenomenon is capable to to the diagnosis of BD including: angiography, nuclear scan, transcranial Doppler sonograpreserve a sufficient blood supply as long as CPP exceeds evoked potentials) or cerebral circulatory arrest. A number of blood flow tests were phy (TCD), computed tomographic angiography (CTA), magapprox. 50 mmHg [5]. Further elevation of ICP results in introduced to the diagnosis of BD including: (MRA), catheterperfusion cerebral angiography, nuclear netic resonance angiography CT (PCT), an increase of CVR. The deep cerebral veins and capillarxenon CT, magnetic resonance magnetic ies as the most susceptible vessels are primarily affected; scan, transcranial Doppler sonography (TCD),perfusion computed(MRP), tomographic angiography resonance spectroscopy (MRS), diffusion-weighted MRI then the process spreads proximally involving bigger arter(CTA), magnetic resonance angiography (MRA), perfusion CT (PCT), xenon ies CT, (DWI) and functional MRI (fMRI). progressively.

magnetic resonance perfusion (MRP), magnetic resonance spectroscopy (MRS), Although catheter angiography is considered as a reference Unfortunately, CTA findings have not been studied in nondiffusion-weighted (DWI) and functional (fMRI). test MRI in the diagnosis of BD theMRI method has major drawbrain-dead patients with intracranial hypertension yet. backs: invasiveness, technical complexity, inability to be Although catheter angiography is considered as a reference test in the diagnosis ofThe BDearliest sign of cerebral circulatory arrest in CTA is a performed at the bedside, and limited accessibility of the lack of opacification of the deep veins – the internal certhe method hasangiographic major drawbacks: technicalnoninvasive complexity, and inability to be veins (ICV) and the great cerebral vein (GCV, vein of labs. invasiveness, Therefore modern, ebral ubiquitous modality like CTA has recently attracted attenGalen). performed at the bedside, and limited accessibility of the angiographic labs. Therefore The sensitivity of this finding in the diagnosis of tion. CTA to the diagnosis of BD was introduced in 1998 by cerebral circulatory arrest in CTA is 98–100% [4,6–8]. A lack modern, noninvasive ubiquitous modality like CTA has recently attracted Dupas etand al. [4]. of opacification of cortical branches of the middle cerebral attention. CTA to the diagnosis of BD was introduced in 1998 by Dupas et al. 4. arteries (MCA-M4) is a slightly less sensitive indicator of CT Angiography Findings in Cerebral Circulatory Arrest cerebral circulatory arrest with a sensitivity of 86–100% [6,7]. The basilar artery (BA) and cortical branches of the CT angiography findings in cerebral circulatory arrest Cerebral blood flow (CBF) is continuously regulated by cerposterior cerebral arteries (PCA-P2) are more frequentCerebralebral blood flow (CBF) is continuously regulated by cerebral perfusion pressure (CPP) and cerebrovascular resist- perfusion ly opacified in cerebral circulatory arrest than MCA-M4. ance (CVR). CPP is measured as a difference between the Their sensitivities are 83–94% and 79%, respectively [4,6,9]. pressure (CPP) and cerebrovascular resistance (CVR). CPP is measured as a entry pressure - mean arterial pressure (MAP) and the The least sensitive finding of cerebral circulatory arrest is difference between the entry -pressure - mean arterial(ICP). pressure (MAP) to and theaexit exit pressure intracranial pressure According lack of opacification of cortical branches of the anterior Poiseuille equation: cerebral artery (ACA-A3, pericallosal artery) with a sensipressure - intracranial pressure (ICP). According to Poiseuille equation: tivity of 64% [6]. Such a sequence is explained by the highMAP - ICP CPP est susceptibility of cortical branches of the MCA to the = CBF = intracranial hypertension and the lowest cerebral perfuCVR CVR sion pressure (CPP) in these arteries – see Figure 1. In the Normal CBF at rest is maintained within a range of 45-60 mL/100g of brain course of cerebral circulatory arrest, proximal segments of tissue/min. A brain injury is accompanied by cerebral edema. Because the skull bones limit the intracranial 418 volume this “mass effect” leads to the intracranial hypertension. The process spreads from the region of primary injury gradually involving the whole brain and the intracranial vessels become compressed but preserve their patency. Initially CVR is kept almost constant by the activated autoregulation mechanisms

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Sawicki M. et al. – CT angiography in the diagnosis of brain death

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Figure 2. Positive results of CTA in the diagnosis of BD: (A) – 10-mm MIP in the coronal plane shows stasis filling with delayed opacification of proximal MCAs (white arrows); please note the simultaneous opacification of the superficial temporal arteries (black arrows) (B) – 10-mm MIP in the coronal plane shows no intracranial filling; these findings confirm the diagnosis of BD. the cerebral arteries may show opacification for some time – Figure 2A. These arteries appear as thin and their filling is delayed and weak [10]. Intracranial stasis of contrast is observed with its extremely slow elimination through arteriovenous shunts and extravasation due to the interrupted blood-brain barrier. The last sign of cerebral circulatory arrest is intracranial non-filling – see Figure 2B.

Technique of CT Angiography in the Diagnosis of Cerebral Circulatory Arrest The technique of CTA involves rapid, intravenous administration of iodinated contrast followed by volume scanning of the whole brain. For the diagnosis of BD, at least 3 acquisitions should be performed: 1. Non-enhanced scanning as a reference for assessing vascular opacification. 2. Early post-contrast scanning for assessing intra- and, which is more important, extracranial vascular opacification. Usually this phase is started 20 sec. after the beginning of injection. Opacification of branches of external carotid arteries – the superficial temporal or the facial arteries indicate that the contrast was injected correctly and there are no hemodynamic abnormalities causing a delay of contrast delivery to the vessels of the head and neck.

Table 1. CTA evaluation scales in the diagnosis of BD. Criteria

Lack of opacification of

Intracranial • ICA beyond the level of the anterior clinoid process non-filling • VA beyond their dural penetration • ICV, GCV and the straight sinus 10-point*

• BA • Right and left PCA-P2 • Right and left ACA-A3 (pericallosal artery) • Right and left MCA-M4 • Right and left ICV • GCV

7-point*

• Right and left ACA-A3 (pericallosal artery) • Right and left MCA-M4 • Right and left ICV • GCV

4-point*

• Right and left MCA-M4 ** • Right and left ICV

* One point is noted for each nonopacified vessel in the late phase. Cerebral circulatory arrest is diagnosed with the score of 10, 7, or 4 points, accordingly; ** according to the 4-point scale, opacification of 1 or 2 cortical branches of MCA on the same side does not exclude the diagnosis of cerebral circulatory arrest provided there is no opacification of ICVs.

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Figure 3. The case of a 30-year-old woman with brain stem hematoma and frontal craniotomy presenting signs of BD on clinical examination; (A) – 10-mm MIP in the sagittal plane in CTA shows opacification of both pericallosal arteries (thin arrows); (B) – 10-mm MIP in the coronal plane in CTA shows opacification of cortical segments of MCAs (thin arrows); these findings exclude the diagnosis of BD. Table 2. Sensitivity of CTA in the diagnosis of BD. Study authors and year

No of cases

Sensitivity (%) 10-point

7-point

4-point

Combes et al. 2007 [15]

43

70

Welschehold et al. 2013 [16]

63

54 *

Dupas et al. 1998 [4]

14

Quesnel et al. 2007 [13]

21

Frampas et al. 2009 [6]

105

63

86

Rieke et al. 2011 [14]

29

76

93

Leclerc et al. 2006 [7]

15

Sawicki et al. 2014 [9]

82

100 52**

87 67

74

96

* GCV was not assessed, ** the study included 5 out of 21 patients with anoxic brain injury. 3. Late post-contrast scanning for assessing intracranial vascular opacification. This phase is started 60 sec. after the beginning of injection, with a delay of 40 sec. to the early phase. The necessity of performing the late phase of CTA in the diagnosis of cerebral circulatory arrest is motivated by a possible delayed vascular opacification in intracranial hypertension. Termination of the study on the early phase may result in a failure to recognize delayed intracranial filling giving a false positive result.

Criteria for the Diagnosis of Cerebral Circulatory Arrest in CT Angiography There are no widely accepted criteria of CTA in the diagnosis of cerebral circulatory arrest. Four methods of evaluation have been proposed so far; they are summarized in Table 1.

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Usefulness of CT Angiography in the Diagnosis of Cerebral Circulatory Arrest CTA is far more widely available than any other blood flow test. The study is noninvasive, technically uncomplicated and non-time consuming. However, CTA cannot be applied at the bedside, while the transport of ICU patients is always insecure. The potential risk of damage of transplantable organs caused by iodinated contrast, although postulated, has not been confirmed yet. Moreover, it was revealed that contrast medium administration to donors does not affect kidney graft function after transplantation [11]. The accuracy of CTA in the diagnosis of cerebral circulatory arrest has not been reliably studied yet. In particular, specificity of the method has not been evaluated with

© Pol J Radiol, 2014; 79: 417-421

non-brain-dead patients with intracranial hypertension as controls. However there are no reports on false positive CTAs involving multiphase scanning. Skull decompression and ischemic-hypoxic injury after cardiac arrest are the predisposing factors to false negative results of CTA [12–14] – see Table 2.

Limitations of CT Angiography in the Diagnosis of Cerebral Circulatory Arrest The limitations of CTA result most of all from uneven distribution of intracranial hypertension in some brain-dead patients due to local decompression of the cranial fossa – see Figure 3. There are several mechanisms causing a local decrease of ICP: craniectomy, ventricular drainage, skull fracture, open fontanelles and unfused sutures in neonates and infants. The regionally decreased ICP may result in preservation or restoration of residual cerebral blood flow at the site of decompression while in the remaining parts of the brain the cessation of blood flow is detected [15,16]. A similar problem can be met in some cases of infratentorial injuries in which the increase of ICP in the subtentorial

Sawicki M. et al. – CT angiography in the diagnosis of brain death

compartment precedes its increase in the supratentorial region due to the protective function of the cerebellar tentorium [14]. In such cases the blood flow in cerebral hemispheres ceases with a marked delay in comparison to the posterior circulation. An opposite sequence is known as well, when cessation of blood flow in the supratentorial region precedes cerebral circulatory arrest in the basilar artery [17]. Diagnostic difficulties are also encountered in case of hypoxic-ischemic brain injuries after cardiac arrest when the ineffective restoration of cerebral blood flow is observed [12,13].

Future Trends CTA is the most promising ancillary test considering the recent introduction of ultrafast, wide detector scanners. Such machines are capable of performing time-resolved dynamic CTA (4D CTA). Combination of 4D CTA with wholebrain PCT using a single contrast injection seems to be the most promising alternative for the future. The problem of portability of CT may be resolved in next years. First portable CT scanners are already on the market.

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2. Wijdicks EF, Varelas PN, Gronseth GS et al: Evidence-based guideline update: determining brain death in adults: report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology, 2010; 74: 1911–18

11. Grosse K, Brauer B, Kucuk O et al: Does contrast medium administration in organ donors affect early kidney graft function? Transplant Proc, 2006; 38: 668–69

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12. Escudero D, Otero J, Marques L et al: Diagnosing brain death by CT perfusion and multislice CT angiography. Neurocrit Care, 2009; 11: 261–71 13. Quesnel C, Fulgencio JP, Adrie C et al: Limitations of computed tomographic angiography in the diagnosis of brain death. Intensive Care Med, 2007; 33: 2129–35 14. Rieke A, Regli B, Mattle HP et al: Computed tomography angiography (CTA) to prove circulatory arrest for the diagnosis of brain death in the context of organ transplantation. Swiss Med Wkly, 2011; 141: w13261 15. Combes JC, Chomel A, Ricolfi F et al: Reliability of computed tomographic angiography in the diagnosis of brain death. Transplant Proc, 2007; 39: 16–20 16. Welschehold S, Kerz T, Boor S et al: Detection of intracranial circulatory arrest in brain death using cranial CT-angiography. Eur J Neurol, 2013; 20(1): 173–79 17. Braun M, Ducrocq X, Huot JC et al: Intravenous angiography in brain death: report of 140 patients. Neuroradiology, 1997; 39: 400–5

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